Plasticity of social organization in a forest ant species

We manipulated availability of food and nesting sites in one population of the forest ant Myrmica punctiventris. The manipulations produced significant changes in relatedness structure, reproductive allocation, and response to hierarchical selection. Food availability appeared to have a consistently stronger influence on these aspects of social organization than did availability of nesting sites. We interpret our experimental results in light of observed differences between populations, and discuss implications for kin selection dynamics. Received: 30 July 1998 / Accepted after revision: 31 October 1998     

Multiple reproductive strategies in a tropical hover wasp

Reproductive skew theory has been an important component of efforts to design a unifying theory of social evolution, as it aims to explain patterns of reproductive partitioning in animal societies as a function of relatedness, group productivity, fighting ability and ecological constraints on independent reproduction. However, empirical tests of the theory have often provided ambiguous or non-conclusive results, assumptions behind alternative models have rarely been tested, and theoretical elaborations have shown the limitations of the reproductive skew approach. Here we analyse a relatively large sample of colonies of the Stenogastrine wasp Parischnogaster mellyi with a powerful set of DNA microsatellite markers. We show that various apparently stable forms of social organisation co-exist in a single population, and that sharing of reproduction between related and unrelated egg-laying females occurs in some of the nests. Present reproductive skew theory appears to be at best partly sufficient to account for the observed complexity of social organisation. The observed patterns of colony composition and reproductive sharing are weakly consistent with the hypothesis of reproductive transactions, while they can more parsimoniously be explained by the life-history characteristics of the species.Communicated by R.F.A. Moritz     

Sociogenetic organization of the red ant Myrmica rubra

Knowledge of the sociogenetic organization determining the kin structure of social insect colonies is the basis for understanding the evolution of insect sociality. Kin structure is determined by the number and relatedness of queens and males reproducing in the colonies, and partitioning of reproduction among them. This study shows extreme flexibility in these traits in the facultatively polygynous red ant Myrmica rubra. Relatedness among worker nestmates varied from 0 to 0.82. The most important reason for this variation was the extensive variation in the queen number among populations. Most populations were moderately or highly polygynous resulting in low relatedness among worker nestmates, but effectively monogynous populations were also found. Polygynous populations also often tend to be polydomous, which is another reason for low relatedness. Coexisting queens were positively related in two populations out of five and relatedness was usually similar among workers in the same colonies. Due to the polydomous colony organization and short life span of queens, it was not possible to conclusively determine the importance of unequal reproduction among coexisting queens, but it did not seem to be important in determining the relatedness among worker nestmates. The estimates of the mating frequency by queens remained ambiguous, which may be due to variation among populations. In some populations relatedness among worker nestmates was high, suggesting monogyny and single mating by queens, but in single-queen laboratory nests relatedness among the worker offspring was lower, suggesting that multiple mating was common. The data on males were sparse, but indicated sperm precedence and no relatedness among males breeding in the same colony. A comparison of social organizations and habitat requirements of M. rubra and closely related M. ruginodis suggested that habitat longevity and patchiness may be important ecological factors promoting polygyny in Myrmica. Received: 15 May 1995/Accepted after revision: 17 October 1995     

Kin conflict over caste determination in social Hymenoptera

We argue that caste determination, the process whereby females in the social Hymenoptera develop into either queens or workers, is subject to kin-selected conflict. Potential conflict arises because developing females are more closely related to their would-be offspring than to those of other females. Therefore, they may favour becoming queens contrary to the interests of other developing females and of existing queens and workers. We suggest two contexts leading to potential caste conflict. The first occurs when queens are reared in a reproductive phase following an ergonomic phase of worker production, while the second occurs when queens and workers are reared simultaneously. The first context assumes that workers' per capita contribution to colony survival and productivity falls with rising colony size. A critical feature influencing whether potential conflict is realized is the extent to which developing females can determine their own caste (“self-determination”). Self-determination is facilitated when female larvae control their own food intake and when queen-worker size dimorphism is low. We know of no strong evidence for actual conflict over caste fate arising in the first context. However, stingless bees and polygynous ants with excess queen-potential larvae that are either forced to develop as workers or are culled as adults demonstrate actual caste conflict in the second context. Caste conflict does not preclude caste regulation for “the good of the colony”, but such regulation is contingent on either the absence of potential conflict or on developing females losing control of their caste fate. Received: 22 March 1999 / Received in revised form: 15 June 1999 / Accepted: 19 June 1999     

Kin-preferential cooperation,dominance-dependent reproductive skew,and competition for mates in communally nesting female house mice

Little is known about the behavioural mechanisms facilitating kin-preferential communal breeding in wild house mice (Mus domesticus). We evaluated the effect of kinship and male availability on aggression, social structure and reproductive skew in groups of female mice freely interacting and reproducing in semi-natural indoor enclosures. Triplets of either sisters or non-sisters were established in enclosures provided with either one or three littermate males, which were unrelated and unfamiliar to the females. Sisters were more spatially associated and less aggressive than non-sisters, leading to higher incidences of communal breeding and reproduction. This is in agreement with theoretical considerations on kin selection in house mice. Reproductive success was highly skewed in favour of dominant females due to subordinate infertility or complete loss of first litters, which might have been caused by dominant females. In spite of this, subordinates only rarely dispersed from the enclosures, suggesting that perceived dispersal risk generally outweighed relatively reduced reproductive potentials. Aggression levels among females were significantly higher when one male was available, compared to when three males were available. We suggest that this might result from higher female-female competition for mates, due to the risk of missing fertilisation when synchronously oestrous females encounter limited numbers of males in a deme. Our results indicate that, first, communal nursing in house mice might have evolved to make the best out of a bad job rather than to enhance offspring fitness; and, second, that female-female mate-competition might play an important role in shaping female social structure in this polygynous mammal.Electronic Supplementary Material Supplementary material is available in the online version of this article at Communicated by F. Trillmich     

Delayed dispersal as a potential route to cooperative breeding in ambrosia beetles

Xyleborini are a species-rich tribe of ambrosia beetles, which are haplodiploid and typically mate among siblings within their natal brood chamber. Several characteristics of this tribe would predict the evolution of higher levels of sociality: high genetic relatedness within galleries due to inbreeding, high costs of dispersal and the potential benefit of cooperation in brood care within the natal gallery (e.g. by fungus gardening, gallery extension, offspring feeding and cleaning). However, information on the social system of these beetles is very limited. We examined the potential for cooperative breeding in Xyleborinus saxeseni by monitoring dispersal in relation to brood size and composition. Results show that adult female offspring delay dispersal despite dispersal opportunities, and apparently some females never disperse. The females’ decision to stay seems to depend on the presence of eggs and dependent siblings. We found no indication that female offspring reproduce in their natal gallery, as colonies with many mature daughters do not contain more eggs than those with few or no daughters. There is a significant positive relationship between the number of females present and the number of dependent siblings (but not eggs), which suggests that cooperative brood care of female offspring raises colony productivity by improving survival rates of immatures. Our results suggest that cooperative breeding is likely to occur in X. saxeseni and possibly other xyleborine species. We argue that a closer look at sociality within this tribe may yield important information on the factors determining the evolution of cooperative breeding and advanced social organization.     

Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control

Reproductive skew models have been proposed as a unifying framework for understanding animal social systems, but few studies have investigated reproductive skew in a broad evolutionary context. We compiled data on the distribution of mating among males for 31 species of primates and calculated skew indices for each study. We analyzed the determinants of mating skew with phylogenetic comparative methods to investigate two models from reproductive skew theory, the concession model and the tug-of-war model. Mating skew decreased as the number of males increased in multimale groups, suggesting that monopolization of females becomes more difficult when there are more rivals, and therefore supporting the tug-of-war model. We predicted that single males are unable to monopolize receptive females as overlap in female receptivity increases (estrous synchrony) and, as a result, that mating skew decreases. However, we did not find any evidence for a link between female estrous synchrony and male mating skew. Finally, the concession model predicts high skew in male philopatric species relative to species in which males disperse, yet our measures of mating skew showed no significant associations with qualitative scores of male dispersal. More definitive tests of the concession model will require more quantitative measures of relatedness, which are presently unavailable for most primate species in our study. Overall, our results provide support for the tug-of-war model in primates, and the approach developed here can be applied to study comparative patterns of skew in other biological systems.Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible to authorized users.     

Patterns of paternity skew in Formica ants

Reproductive skew among cooperatively breeding animals has recently attracted considerable interest. In social insects reproductive skew has been studied in females but not in males. However, cooperative breeding of males occurs when two males mate with the same queen and father offspring. Here we present the first analysis of comparative data on paternity skew in ants. We show that, across seven species of Formica ants, the average skew in paternity among worker offspring of doubly mated queens is negatively correlated with the population-wide frequency of multiple (mostly double) mating. We also demonstrate that this trend is relatively robust in additional analyses taking phylogenetic relationships between species into account. The observed trend is opposite to the one normally found in non-social insects with second-male precedence through sperm displacement, but agrees with predictions based on queen-male conflict over sperm allocation as a consequence of facultative, worker controlled, sex allocation – an interpretation which assumes first-male precedence. However, alternative (but not mutually exclusive) explanations are possible and further studies will be needed to discriminate between these alternatives. Received: 16 May 1997 / Accepted after revision: 26 September 1997     

Kin associations and direct vs indirect fitness benefits in colonial cooperatively breeding sociable weavers Philetairus socius

Indirect fitness benefits are believed to be an important force behind the evolution of cooperative breeding. However, helpers may associate with their relatives as a result of delayed dispersal, hence, kin associations might be a consequence of demographic viscosity rather than active choice. In addition, recent studies showed that helpers may have access to reproduction therefore direct benefits might also play an important role. Here, we investigate the possible roles of direct genetic benefits and kin associations on helping behavior in the sociable weaver Philetairus socius, a colonial and cooperatively breeding passerine. We used a microsatellite-based genotyping method to describe the genetic structure within nests and colonies. Within a colony, we found considerable genetic structure between males but not females. Sociable weaver colonies have several nests that are simultaneously active, giving individuals a choice of associating with a range of first-order kin to unrelated individuals. Helpers were significantly more related to the young in the helped nests than in other nests of the colony, suggesting an active choice for associating with kin. The helpers were generally offspring or first-order relatives of one (50%) or both (43%) breeders, although more infrequently, seemingly unrelated individuals also helped (7%). We found no supporting evidence of extrapair parentage and hence no direct genetic gains from helping in our population. This strong reproductive skew is contrary to theoretical models predicting conflicts over reproduction in stepfamilies. We discuss whether female decisions and/or other direct benefits of remaining in kin associations or helping might explain the high skew observed.     

Female control of reproductive skew in cooperatively breeding brown jays (<Emphasis Type="Italic">Cyanocorax morio</Emphasis>)

Brown jays (Cyanocorax morio) are long-lived, social corvids that live in large, stable, territorial groups (mean = 10 individuals). In this study, I determined the distribution of reproductive success within groups using multi-locus DNA fingerprinting. Breeding females produced virtually all (99%) of the young within their own nests. Reproduction within groups was highly skewed towards a single primary female, although long term data indicate that secondary females (female breeders that were usually younger and subordinate to the primary female) were sometimes successful. The high reproductive skew observed for females was associated with primary female aggression. Successful reproduction by secondary females may have been due to parental facilitation or the inability of primary females to completely suppress secondary females. Multiple paternity occurred in 31–43% of broods and extra-group paternity occurred in a minimum of 22% of broods. Patterns of paternity also varied between years, since females often switched or included new genetic mates. Although male consorts of nesting females fathered relatively few offspring (20%), they still had a higher chance of fathering offspring than any other single group male. Reproduction was less skewed for males than females as a result of female mating patterns. Female reproductive patterns are consistent with some of the predictions and assumptions from optimal skew models, while male reproductive patterns are not. The factors affecting skew in species with complex social systems such as incomplete control by breeders over subordinate reproduction, female control of paternity, and resource inheritance have not been well incorporated into reproductive skew models.Communicated by: J. Dickinson     

The lemur syndrome unresolved: extreme male reproductive skew in sifakas (<Emphasis Type="Italic">Propithecus verreauxi</Emphasis>), a sexually monomorphic primate with female dominance

The primates of Madagascar (Lemuriformes) are unusual among mammals in that polygynous species lack sexual dimorphism, and females dominate males socially in most species. Moreover, lemur groups are relatively small and characterized by even adult sex ratios despite the fact that one male should be able to exclude other males from the group. One hypothesis to explain this combination of behavioral, morphological, and demographic traits (the “lemur syndrome”) postulates that male–male competition is relaxed and, hence, variance in male reproductive success is low. Reproductive skew theory provides a framework for testing this and several related predictions about lemur social evolution. Specifically, low reproductive skew is also predicted if dominant males or adult females make reproductive concessions to subordinates or if the latter group successfully pursues alternative reproductive tactics. However, suitable data on paternity, demography, and behavior for a conclusive test of these predictions have not been available in the past. In this paper, we show that male reproductive success in ten groups of Verreaux’s sifakas (Propithecus verreauxi) was extremely skewed in favor of the dominant male over 9 years. Our genetic analyses also revealed that more than a third of all groups are effectively harem groups because only one male was unrelated to the resident female(s). In groups with two or more non-natal males, the dominant sired 91% of 33 infants. Together, males pursuing one of several alternative reproductive tactics, such as roaming among several groups or immigrating peacefully, sired only 11% of infants. Thus, female sifakas do not control group composition by offering reproductive opportunities to subordinate males as staying incentives, intrasexual selection is not relaxed, and dominant males prevail in a tug-of-war over subordinate males. Because male reproductive skew in sifakas is even more pronounced than in harem-living anthropoids studied to date, intrasexual selection is clearly not relaxed, and the lemur syndrome is more puzzling than ever.     

Reproductive success in a low skew, communal breeding mammal: the banded mongoose, Mungos mungo

In most cooperatively breeding species, reproduction is monopolised by a subset of group members. However, in some species most or all individuals breed. The factors that affect reproductive success in such species are vital to understanding why multiple females breed. A key issue is whether or not the presence of other breeders is costly to an individual’s reproductive success. This study examines the factors that affect the post-parturition component of reproductive success in groups of communal-breeding banded mongoose (Mungos mungo), where up to ten females breed together. Per-litter reproductive success was low (only 18% of pups survived from birth to independence). Whilst singular breeding was wholly unsuccessful, there were costs associated with breeding in the presence of increasing numbers of other females and in large groups. Synchronisation of parturition increased litter success, probably because it minimises the opportunity for infanticide or decreases competitive asymmetry between pups born to different females. There was no evidence of inbreeding depression, and reproductive success was generally higher in litters where females only had access to related males within their group. I conclude that communal breeding in female banded mongooses represents a compromise between the benefits of group-living and communal pup care on the one hand, and competition between females to maximise their personal reproductive success on the other. Such conflicts are likely to occur in most communal breeding species. Whilst communal breeding systems are generally considered egalitarian, negative effects of co-breeders on individual reproductive success is still an issue.     

Lack of detectable nepotism in multiple-queen colonies of the fire ant Solenopsis invicta (Hymenoptera: Formicidae)

Multiple-queen (polygyne) colonies of the introduced fire ant Solenopsis invicta present a paradox for kin selection theory. Egg-laying queens within these societies are, on average, unrelated to one another, and the numbers of queens per colony are high, so that workers appear to raise new sexuals that are no more closely related to them than are random individuals in the population. This paradox could be resolved if workers discriminate between related and unrelated nestmate sexuals in important fitness-related contexts. This study examines the possibility of such nepotism using methods that combine the following features: (1) multiple relevant behavioral assays, (2) colonies with an unmanipulated family structure, (3) multiple genetic markers with no known phenotypic effects, and (4) a statistical technique for distinguishing between nepotism and potentially confounding phenomena. We estimated relatedness between interactants in polygyne S. invicta colonies in two situations, workers tending egg-laying queens and workers feeding maturing winged queens. In neither case did we detect a significant positive value of relatedness that would implicate nepotism. We argue that the non-nepotistic strategies displayed by these ants reflect historical selection pressures experienced by native populations, in which nestmate queens are highly related to one another. The markedly different genetic structure in native populations may favor the operation of stronger higher-level selection that effectively opposes weaker individual-level selection for nepotistic interactions within nests. Received: 28 June 1996 / Accepted after revision: 6 October 1996     

Levels of selection in a social insect: a review of conflict and cooperation during honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) queen replacement

The extended phenotype of a social insect colony enables selection to act at both the individual level (within-colony selection) and the colony level (between-colony selection). Whether a particular trait persists over time depends on the relative within- and between-colony selection pressures. Queen replacement in honey bee colonies exemplifies how selection may act at these different levels in opposing directions. Normally, a honey bee colony has only one queen, but a colony rears many new queens during the process of colony reproduction. The replacement of the mother queen has two distinct phases: queen rearing, where many queens develop and emerge from their cells, and queen elimination, where most queens die in a series of fatal duels. Which queens are reared to adulthood and which queens ultimately survive the elimination process depends on the strength and direction of selection at both the individual and colony levels. If within-colony selection is predominant, then conflict is expected to occur among nestmates over which queens are produced. If between-colony selection is predominant, then cooperation is expected among nestmates. We review the current evidence for conflict and cooperation during queen replacement in honey bees during both the queen rearing and queen elimination phases. In particular, we examine whether workers of different subfamilies exhibit conflict by acting nepotistically toward queens before and after they have emerged from their cells, and whether workers exhibit cooperation by collectively producing queens of high reproductive quality. We conclude that although workers may weakly compete through nepotism during queen rearing, workers largely cooperate to raise queens of similar reproductive potential so that any queen is suitable to inherit the nest. Thus it appears that potential conflict over queen replacement in honey bees has not translated into actual conflict, suggesting that between-colony selection predominates during these important events in a colonys life cycle.Communicated by A. Cockburn     

Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula

Social Hymenoptera are general models for the study of parent-offspring conflict over sex ratio, because queens and workers frequently have different reproductive optima. The ant Pheidole pallidula shows a split distribution of sex ratios with most of the colonies producing reproductives of a single sex. Sex ratio specialization is tightly associated with the breeding system, with single-queen (monogynous) colonies producing male-biased brood and multiple-queen (polygynous) colonies female-biased brood. Here, we show that this sex specialization is primarily determined by the queens influence over colony sex ratio. Queens from monogynous colonies produce a significantly more male-biased primary sex ratio than queens from polygynous colonies. Moreover, queens from monogynous colonies produce a significantly lower proportion of diploid eggs that develop into queens and this is associated with lower rate of juvenile hormone (JH) production compared to queens from polygynous colonies. These results indicate that queens regulate colony sex ratio in two complementary ways: by determining the proportion of female eggs laid and by hormonally biasing the development of female eggs into either a worker or reproductive form. This is the first time that such a dual system of queen influence over colony sex ratio is identified in an ant.     

Intraspecific parasitism and split sex ratios in a monogynous and monandrous ant (Leptothorax nylanderi)

Sex ratios were bimodally distributed in a population of the monogynous and monandrous ant Leptothorax nylanderi during each of 3 study years. The population-wide investment ratios suggested worker control of sex allocation. Nest-level variation in the proportional investment in virgin queens was not affected by the presence or absence of a queen and only slightly by collecting year, but was correlated with nest size, total sexual investment and, unexpectedly, with differences in nestmate relatedness: small, low-investment nests and nests with several worker lineages produced male-biased sex ratios. Colonies containing several worker lineages arise from usurpation of mature colonies by unrelated founding queens and the fusion of unrelated colonies under strong nest site limitation. In contrast to facultatively polygynous and polyandrous species of social insects, where workers can maximize their inclusive fitness by adjusting sex ratios according to the degree of relatedness asymmetry, workers in mixed colonies of L. nylanderi do not benefit from manipulating sex allocation, as here relatedness asymmetries appear to be the same as in homogeneous colonies. Received: 7 December 1999 / Received in revised form: 29 February 2000 / Accepted: 13 March 2000     

Effects of paternal care on reproductive success in the polygynous spotless starling Sturnus unicolor

For males of socially polygynous avian species like the spotless starling, there may exist a trade-off between investing in paternal care and controlling several nests. To determine how the intensity of paternal care affects reproductive success per brood sired or expressed as the total number of young raised in all nests controlled by the same male, it is necessary to manipulate paternal care. Testosterone (T) has been shown to depress the tendency for males to care for their young, and induces them to acquire more mates. The effects of paternal care on reproductive success were studied by treating certain male starlings with exogenous T and others with the antiandrogen cyproterone acetate (CA), and comparing the parental behavior of T- and CA-males throughout the breeding season with that of controls. CA-males fed their chicks more during the first week after hatching than T-males, with controls feeding at intermediate rates, both on a per nest basis and as total effort for all nests controlled by the same male. Paternal feeding rates during the first week of chick life had a significant positive effect on the number of fledged young. The hormone treatment significantly affected the number of chicks raised per nest, CA-males having a higher breeding success per nest than T-males, and controls showing intermediate levels of success. There was no significant effect of treatment on total reproductive success attained by males throughout the season. In the polygonous spotless starling, the intensity of paternal care of young affects reproductive success per nest positively but not on a seasonal basis. Received: 6 February 1999 / Received in revised form: 30 June 1999 / Accepted: 11 July 1999     

Social relationships among adult female baboons (Papio cynocephalus) II. Variation in the quality and stability of social bonds

A growing body of evidence suggests that social bonds have adaptive value for animals that live in social groups. Although these findings suggest that natural selection may favor the ability to cultivate and sustain social bonds, we know very little about the factors that influence the quality or stability of social bonds. Here, we draw on data derived from a 16-year study of baboons living in seven different social groups in the Amboseli basin of Kenya to evaluate the quality and stability of social bonds among females. Our results extend previous analyses, which demonstrate that females form the strongest bonds with close maternal and paternal kin, age mates (who may be paternal kin), and females who occupy similar ranks but are not maternal relatives. Here we show that the same factors influence the quality and strength of social bonds. Moreover, the results demonstrate that the quality of social bonds directly affects their stability.     

Young-boy networks without kin clusters in a lek-mating manakin

I use 10 years of data from a long-term study of lek-mating long-tailed manakins to relate the social network among males to their spatial and genetic structure. Previously, I showed that the network connectivity of young males predicts their future success. Here, I ask whether kinship might shape the organization of this “young-boy network”. Not surprisingly, males that were more socially distant (linked by longer network paths) were affiliated with perch zones (lek arenas) that were further apart. Relatedness (r) among males within the network decreased as social distance increased, as might be expected under kin selection. Nevertheless, any role for indirect inclusive fitness benefits is refuted by the slightly negative mean relatedness among males at all social distances within the network (overall mean r = −0.06). That is, relatedness ranged from slightly negative (−0.04) to more negative (−0.2). In contrast, relatedness in dyads for which at least one of the males was outside the social network (involving at least one blood-sampled male not documented to have interacted with other banded males) was slightly above the random expectation (mean r = 0.05). The slight variations around r = 0 among males of different categories likely reflect dispersal dynamics, rather than any influence of kinship on social organization. Relatedness did not covary with the age difference between males. These results, together with previous results for lack of relatedness between alpha and beta male partners, refute any role for kin selection in the evolution of cooperative display in this lek-mating system. This contribution is part of the special issue “Social Networks: new perspectives” (Guest Editors: J. Krause, D. Lusseau, and R. James).     

Extended family structure in the ant Formica paralugubris: the role of the breeding system

In populations of various ant species, many queens reproduce in the same nest (polygyny), and colony boundaries appear to be absent with individuals able to move freely between nests (unicoloniality). Such societies depart strongly from a simple family structure and pose a potential challenge to kin selection theory, because high queen number coupled with unrestricted gene flow among nests should result in levels of relatedness among nestmates close to zero. This study investigated the breeding system and genetic structure of a highly polygynous and largely unicolonial population of the wood ant Formica paralugubris. A microsatellite analysis revealed that nestmate workers, reproductive queens and reproductive males (the queens' mates) are all equally related to each other, with relatedness estimates centring around 0.14. This suggests that most of the queens and males reproducing in the study population had mated within or close to their natal nest, and that the queens did not disperse far after mating. We developed a theoretical model to investigate how the breeding system affects the relatedness structure of polygynous colonies. By combining the model and our empirical data, it was estimated that about 99.8% of the reproducing queens and males originated from within the nest, or from a nearby nest. This high rate of local mating and the rarity of long-distance dispersal maintain significant relatedness among nestmates, and contrast with the common view that unicoloniality is coupled with unrestricted gene flow among nests. Received: 8 February 1999 / Received in revised form: 15 June 1999 / Accepted: 19 June 1999